Perisomatic GABAergic synapses of basket cells effectively control principal neuron activity in amygdala networks.

Judit M Veres,Gergő A Nagy,Norbert Hájos

doi:10.7554/elife.20721

Judit M Veres, Gergő A Nagy + Show 1 more

Open Access

https://doi.org/10.7554/elife.20721

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Abstract

Efficient control of principal neuron firing by basket cells is critical for information processing in cortical microcircuits, however, the relative contribution of their perisomatic and dendritic synapses to spike inhibition is still unknown. Using in vitro electrophysiological paired recordings we reveal that in the mouse basal amygdala cholecystokinin- and parvalbumin-containing basket cells provide equally potent control of principal neuron spiking. We performed pharmacological manipulations, light and electron microscopic investigations to show that, although basket cells innervate the entire somato-denditic membrane surface of principal neurons, the spike controlling effect is achieved primarily via the minority of synapses targeting the perisomatic region. As the innervation patterns of individual basket cells on their different postsynaptic partners show high variability, the impact of inhibitory control accomplished by single basket cells is also variable. Our results show that both basket cell types can powerfully regulate the activity in amygdala networks predominantly via their perisomatic synapses.

Highlights

Perisomatic region of cortical principal neurons (PNs), comprising the cell body, proximal dendrites and the axon initial segment, is a subcellular domain that is a critical site for the input integration and for the generation of the action potential, the output of neurons
We found that cholecystokinin-expressing basket cells (CCKBCs) and Parvalbumin-containing basket cells (PVBCs) innervated their postsynaptic partners with similar number of boutons (Figure 4G), the average distance of the innervation along the dendritic tree (Figure 4H), the number of the contacts established on the perisomatic region (Figure 4I) and the ratio of perisomatic contacts among all boutons showed no significant difference (Figure 4J, all M-W test, p>0.05)
Our major findings are as follows: (1) CCKBCs and PVBCs provide potent inhibitory control of PN spiking in the BA. (2) Inhibitory synapses originating from the basket cells (BCs) cover the entire somatodendritic membrane surface of PNs and only one third of the BC contacts is established on the perisomatic region on average

Summary

Introduction

Perisomatic region of cortical principal neurons (PNs), comprising the cell body, proximal dendrites and the axon initial segment, is a subcellular domain that is a critical site for the input integration and for the generation of the action potential, the output of neurons. Two major types of GABAergic cells are known to innervate the perisomatic region in all cortical areas: axo-axonic cells form synapses exclusively on the axon initial segment of PNs, while basket cells (BCs) target the soma and proximal dendrites (Somogyi et al, 1983; Somogyi, 1977; Veres et al, 2014; Gulyas et al, 1993). The latter interneuron type is usually divided into two groups by the mutually exclusive expression of neurochemical markers: the calcium binding protein parvalbumin (PV) and the neuropeptide cholecystokinin (CCK). In an influential review it has been proposed that these GABAergic cells may provide a modulatory effect on network dynamics

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